Probabilistic electrical stimulation mapping of human medial frontal cortex

Abstract

The medial frontal cortex remains functionally ill-understood; this is reflected by the heterogeneity of behavioural outcomes following damage to the region. We aim to use the rich information provided by extraoperative direct electrical cortical stimulation to enhance our understanding of its functional anatomy.Examining a cohort of 38 epilepsy patients undergoing direct electrical cortical stimulation in the context of presurgical evaluation, we reviewed stimulation findings and classified them in a behavioural framework (positive motor, negative motor, somatosensory, speech disturbances, and “other”). The spatially discrete cortical stimulation-derived data points were then transformed into continuous probabilistic maps, thereby enabling the voxel-wise spatial inference widely used in the analysis of functional and structural imaging data.A functional map of stimulation findings of the medial wall emerged. Positive motor responses occurred in 141 stimulations (31.2%), anatomically located on the paracentral lobule (threshold at p<.05), extending no further than the vertical anterior commissure (VCA) line. Thirty negative motor responses were observed (6.6%), localised to the VCA line (at p < .001 uncorrected). In 43 stimulations (9.5%) a somatosensory response localised to the caudal cingulate zone (at p < .001 uncorrected), with a second region posterior to central sulcus. Speech disturbances were elicited in 38 stimulations (8.4%), more commonly but not exclusively from the language fMRI dominant side, just anterior to VCA (p < .001 uncorrected). In only 2 stimulations, the patient experienced a subjective “urge” to move in the absence of overt movement.Classifying motor behaviour along the dimensions of effector, and movement vs arrest, we derive a wholly data-driven stimulation map of the medial wall, powered by the largest number of stimulations of the region reported (n = 452) in patients imaged with MRI. This model and the underlying data provide a robust framework for understanding the architecture of the region through the joint analysis of disruptive and correlative anatomical maps.

The role of the cingulate cortex in the generation of motor tics and the experience of the premonitory urge-to-tic in Tourette syndrome

“…This has led some authors to conclude that the mid cingulate cortex plays an important role in the generation/representation of premonitory urges (e.g., O'Neill et al, 2019) whereas others have speculated that the role of the cingulate motor area may be to select/generate a particular action in response to PU that may be primarily generated elsewhere, most likely within the anterior insula (Jackson, Parkinson, Kim, et al, 2011). This latter view is consistent with recent studies demonstrating that while electrical stimulation of medial wall regions of cortex, including the mid cingulate cortex, was sufficient to induce movements, including goal-directed actions, there was no evidence that electrical stimulation of this region induced a phenomenological experience of an 'urge-to-move' (Caruana, Gerbella, Avanzini, Gozzo, Pelliccia, Mai, Abdollahi, Cardinale, Sartori, Lo Russo, Rizzolatti, 2018;Trevisi, Eickhoff, Chowdhury, Jha, Rodionov, Nowell, Miserocchi, McEvoy, Nachev, Diehl, 2018; although see Fried, Katz, McCarthy, Sass, Williamson, Spencer, Spencer, 1991, for an alternative report that electrical stimulation of the posterior SMA can induce the experience of an 'urge-to-move'). In the current study we focus specifically on the relationship between the cingulate cortex, measured using structural magnetic resonance imaging together with the analysis of structural covariance networks, and clinical measures of tic severity and PU.…”

“…By contrast, the PCC and was generally unresponsive in this study when stimulated (Caruana, et al, 2018). However, in another study of electrical stimulation of the medial wall in humans, it was found that stimulation of the caudal cingulate zone (corresponding to the posterior MCC) produced primarily somatosensory responses (primarily paraesthesias, dysesthesias, or pain) but not overt movement (Trevisi et al, 2018). These findings are broadly consistent with our finding that: reduction of GM volume in the MCC region is associated with increased motor tic severity and premonitory urge scores; increases in GM volume in the PCC and aMCC were associated with increased motor tic severity; and increases in GM volume in the aMCC region were associated with increased premonitory sensory phenomena.…”

Language Mapping Using Stereo Electroencephalography: A Review and Expert Opinion

“…As this structure is not included in the classical language network models, Ardila et al (2016) speculated a role in language coordination while Afif et al (2010) underlined the role of the insular middle short gyrus in speech production. A recent sEEG study reported speech arrest after medial frontal ECS sometimes associated with positive or negative motor phenomena of the mouth or tongue ( Trevisi et al, 2018 ). These findings supports a phonological-articulatory network between supplementary motor area and ALA ( Hertrich et al, 2016 ).…”

Stimulation Mapping Using Stereoelectroencephalography: Current and Future Directions

“…One such area of research would include better defining the electrophysical properties most conducive to stimulation mapping, such as the biophysical properties of the cortical regions or the optimal charge density to minimize tissue damage (1,44). Other investigations into optimal stimulation paradigms and excitation properties of certain cortical or subcortical areas could benefit our understanding of both normal regional physiology and pathologic excitability (45)(46)(47)(48). Such investigations could include high-/low-frequency stimulation paradigms or rely on SPES (49)(50)(51)(52).…”

“…The use of SEEG stimulation for these purposes will continue to expand. Recent investigations with human subjects have looked at the function of the prefrontal cortex (56), the frontal operculum (57), medial frontal lobe (47), cingulate cortex (58,59), the fusiform gyrus (60)(61)(62), the insula (63,64), the amygdala (65,66), parietal cortex (67), the anterior thalamus (68), the pulvinar (69), and the claustrum (70). Other investigations have looked at multiple brain regions simultaneously, such as when investigating sleep (71,72).…”